Recombinant cannabinoid type 2 receptor in liposome model activates G protein in response to anionic lipid constituents

Journal of Biological Chemistry

Volumn 287, Issue 6, 2012, Pages 4076-4087

  Kimura, Tomohiro ^a   Yeliseev, Alexei A ^a   Vukoti, Krishna ^a   Rhodes, Steven D ^a   Cheng, Kejun ^a   Rice, Kenner C ^a   Gawrisch, Klaus ^a  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADSORBENT COLUMNS; ANIONIC LIPIDS; CLASS A; ELECTRIC SURFACE POTENTIAL; FUNCTIONAL FORMS; G PROTEIN; G PROTEIN ACTIVATION; HYDROCARBON CHAINS; ISOPYCNIC GRADIENT; MAGIC ANGLE SPINNING NMR; MEAN DIAMETER; MIXED MICELLES; MOLAR RATIO; PHOSPHOCHOLINE; PROTEOLIPOSOMES; QUANTITATIVE BINDING; STRUCTURAL STUDIES; ULTRACENTRIFUGATION;

AMINO ACIDS; CENTRIFUGATION; CRITICAL MICELLE CONCENTRATION; ESCHERICHIA COLI; HYDROCARBON REFINING; HYDROCARBONS; LIPID BILAYERS; SIGNAL TRANSDUCTION;

RECOMBINANT PROTEINS;

2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; CANNABINOID 2 RECEPTOR; CHOLESTEROL; CHOLESTEROL HYDROGEN SUCCINATE; GUANINE NUCLEOTIDE BINDING PROTEIN; LIPID; LIPOSOME; PHOSPHATIDYLSERINE; RECOMBINANT PROTEIN;

ARTICLE; CONTROLLED STUDY; CRITICAL MICELLE CONCENTRATION; ELECTRIC POTENTIAL; ESCHERICHIA COLI; LIPID BILAYER; MICELLE; MOLECULAR SIZE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION;

CHOLESTEROL ESTERS; CYCLOHEXANOLS; GTP-BINDING PROTEINS; HUMANS; LIPOSOMES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PHOSPHOLIPIDS; RECEPTOR, CANNABINOID, CB2; RECOMBINANT PROTEINS;

ESCHERICHIA COLI;

EID: 84856711972     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.268425     Document Type: Article

References (79)

1. Cabral, G. A., and Griffin-Thomas, L. (2009) Emerging role of the cannabinoid receptor CB2 in immune regulation. Therapeutic prospects for neuroinflammation. Expert Rev. Mol. Med. 11, e3
2. Núñez, E., Benito, C., Pazos, M. R., Barbachano, A., Fajardo, O., González, S., Tolón, R. M., and Romero, J. (2004) Cannabinoid CB2 receptors are expressed by perivascular microglial cells in the human brain. An immunohistochemical study. Synapse 53, 208-213 (Pubitemid 39045539)
3. Mechoulam, R., Ben-Shabat, S., Hanus, L., Ligumsky, M., Kaminski, N. E., Schatz, A. R., Gopher, A., Almog, S., Martin, B. R., Compton, D. R., Pertwee, R. G., Griffin, G., Bayewitch, M., Barg, J., and Vogel, Z. (1995) Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem. Pharmacol. 50, 83-90
4. Devane, W. A., Hanus, L., Breuer, A., Pertwee, R. G., Stevenson, L. A., Griffin, G., Gibson, D., Mandelbaum, A., Etinger, A., and Mechoulam, R. (1992) Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258, 1946-1949 (Pubitemid 23026736)
5. Sugiura, T., Kondo, S., Sukagawa, A., Nakane, S., Shinoda, A., Itoh, K., Yamashita, A., and Waku, K. (1995) 2-Arachidonoylglycerol. A possible endogenous cannabinoid receptor ligand in brain. Biochem. Biophys. Res. Commun. 215, 89-97
6. Pacher, P., Bátkai, S., and Kunos, G. (2006) The endocannabinoid system as an emerging target of pharmacotherapy. Pharmacol. Rev. 58, 389-462 (Pubitemid 44394908)
7. Miller, A. M., and Stella, N. (2008) CB2 receptor-mediated migration of immune cells. It can go either way. Br. J. Pharmacol. 153, 299-308
8. Ibrahim, M. M., Deng, H., Zvonok, A., Cockayne, D. A., Kwan, J., Mata, H. P., Vanderah, T. W., Lai, J., Porreca, F., Makriyannis, A., and Malan, T. P., Jr. (2003) Activation of CB2 cannabinoid receptors by AM1241 inhibits experimental neuropathic pain: pain inhibition by receptors not present in the CNS. Proc. Natl. Acad. Sci. U.S.A. 100, 10529-10533 (Pubitemid 37071912)
9. Ibrahim, M. M., Porreca, F., Lai, J., Albrecht, P. J., Rice, F. L., Khodorova, A., Davar, G., Makriyannis, A., Vanderah, T. W., Mata, H. P., and Malan, T. P., Jr. (2005) CB2 cannabinoid receptor activation produces antinociception by stimulating peripheral release of endogenous opioids. Proc. Natl. Acad. Sci. U.S.A. 102, 3093-3098 (Pubitemid 40299921)
10. Jackson, M. L., and Litman, B. J. (1985) Rhodopsin-egg phosphatidylcholine reconstitution by an octyl glucoside dilution procedure. Biochim. Biophys. Acta 812, 369-376
11. Baker, M. (2010) Structural biology. The gatekeepers revealed. Nature 465, 823-826
12. 2 adrenergic receptor-Gs protein complex. Nature 477, 549-555
13. Yeliseev, A., Zoubak, L., and Gawrisch, K. (2007) Use of dual affinity tags for expression and purification of functional peripheral cannabinoid receptor. Protein Expr. Purif. 53, 153-163 (Pubitemid 46283465)
14. Calandra, B., Tucker, J., Shire, D., and Grisshammer, R. (1997) Expression in Escherichia coli and characterization of the human central CB1 and peripheral CB2 cannabinoid receptors. Biotechnol. Lett. 19, 425-428 (Pubitemid 27243846)
15. Yeliseev, A. A., Wong, K. K., Soubias, O., and Gawrisch, K. (2005) Expression of human peripheral cannabinoid receptor for structural studies. Protein Sci. 14, 2638-2653 (Pubitemid 41395590)
16. Krepkiy, D., Gawrisch, K., and Yeliseev, A. (2007) Expression and purification of CB2 for NMR studies in micellar solution. Protein Pept. Lett. 14, 1031-1037 (Pubitemid 350164242)
17. Schubert, R. (2003) Liposome preparation by detergent removal. Methods Enzymol. 367, 46-70
18. Rigaud, J. L., and Lévy, D. (2003) Reconstitution of membrane proteins into liposomes. Methods Enzymol. 372, 65-86
19. Silvius, J. R. (1992) Solubilization and functional reconstitution of biomembrane components. Annu. Rev. Biophys. Biomol. Struct. 21, 323-348
20. Eytan, G. D. (1982) Use of liposomes for reconstitution of biological functions. Biochim. Biophys. Acta 694, 185-202
21. Kimura, T., Cheng, K., Rice, K. C., and Gawrisch, K. (2009) Location, structure, and dynamics of the synthetic cannabinoid ligand CP-55,940 in lipid bilayers. Biophys. J. 96, 4916-4924
22. Herrmann, K. W. (1962) Non-ionic-cationic micellar properties of dimethyldodecylamine oxide. J. Phys. Chem. 66, 295-300
23. Chattopadhyay, A., and Harikumar, K. G. (1996) Dependence of critical micelle concentration of a zwitterionic detergent on ionic strength. Implications in receptor solubilization. FEBS Lett. 391, 199-202 (Pubitemid 26325743)
24. VanAken, T., Foxall-VanAken, S., Castleman, S., and Ferguson-Miller, S. (1986) Alkyl glycoside detergents. Synthesis and applications to the study of membrane proteins. Methods Enzymol. 125, 27-35
25. Mumby, S. M., and Linder, M. E. (1994) Heterotrimeric 6 Proteins (Iyengar, R., ed) pp. 254-268, Academic Press, New York
26. Wildman, D. E., Tamir, H., Leberer, E., Northup, J. K., and Dennis, M. (1993) Prenyl modification of guanine nucleotide regulatory protein γ2 subunits is not required for interaction with the transducin α subunit or rhodopsin. Proc. Natl. Acad. Sci. U.S.A. 90, 794-798 (Pubitemid 23053896)
27. Aveyard, R., and Haydon, D. A. (1973) An Introduction to the Principles of Surface Chemistry, Cambridge University Press, London
28. Davis, J. H., Jeffrey, K. R., Bloom, M., Valic, M. I., and Higgs, T. P. (1976) Quadrupolar echo deuteron magnetic-resonance spectroscopy in ordered hydrocarbon chains. Chem. Phys. Lett. 42, 390-394
29. Jackson, M. L., and Litman, B. J. (1982) Rhodopsin-phospholipid reconstitution by dialysis removal of octyl glucoside. Biochemistry 21, 5601-5608
30. De Grip, W. J., Olive, J., and Bovee-Geurts, P. H. M. (1983) Reversible modulation of rhodopsin photolysis in pure phosphatidylserine membranes. Biochim. Biophys. Acta 734, 168-179 (Pubitemid 13015974)
31. De Grip, W. J., Vanoostrum, J., and Bovee-Geurts, P. H. (1998) Selective detergent-extraction from mixed detergent/lipid/protein micelles, using cyclodextrin inclusion compounds. A novel generic approach for the preparation of proteoliposomes. Biochem. J. 330, 667-674 (Pubitemid 28111960)
32. 2-adrenergic receptors utilizing selfassembling Nanodisc technology. BioTechniques 40, 601-602, 604, 606
33. Sarramegn, V., Muller, I., Milon, A., and Talmont, F. (2006) Recombinant Gprotein-coupled receptors from expression to renaturation.Achallenge towards structure. Cell. Mol. Life Sci. 63, 1149-1164 (Pubitemid 43939002)
34. 2 adrenoceptor binding site with catechol reveals differences in binding and activation by agonists and partial agonists. J. Biol. Chem. 280, 22165-22171
35. Whorton, M. R., Bokoch, M. P., Rasmussen, S. G., Huang, B., Zare, R. N., Kobilka, B., and Sunahara, R. K. (2007) A monomeric G protein-coupled receptor isolated in a high-density lipoprotein particle efficiently activates its G protein. Proc. Natl. Acad. Sci. U.S.A. 104, 7682-7687 (Pubitemid 47185966)
36. 2-adrenoceptor. Insights from fluorescence resonance energy transfer studies. J. Biol. Chem. 282, 13895-13905
37. Niu, S. L., Doctrow, B., and Mitchell, D. C. (2009) Rhodopsin activity varies in proteoliposomes prepared by different techniques. Biochemistry 48, 156-163
38. Watts, A., Volotovski, I. D., and Marsh, D. (1979) Rhodopsin-lipid associations in bovine rod outer segment membranes. Identification of immobilized lipid by spin labels. Biochemistry 18, 5006-5013 (Pubitemid 10204654)
39. Soubias, O., Polozov, I. V., Teague, W. E., Yeliseev, A. A., and Gawrisch, K. (2006) Functional reconstitution of rhodopsin into tubular lipid bilayers supported by nanoporous media. Biochemistry 45, 15583-15590 (Pubitemid 46032479)
40. 15N-MAS NMR and molecular dynamics simulations. Biophys. J. 98, 625a
41. Messerschmidt, A., and Huber, R. (2007) X-Ray Diffraction of Biological Macromolecules, Wiley-VCH, Weinheim, Germany
42. Koenig, B. W., and Gawrisch, K. (2005) Specific volumes of unsaturated phosphatidylcholines in the liquid crystalline lamellar phase. Biochim. Biophys. Acta 1715, 65-70 (Pubitemid 41161161)
43. Heerklotz, H., and Tsamaloukas, A. (2006) Gradual change or phase transition. Characterizing fluid lipid-cholesterol membranes on the basis of thermal volume changes. Biophys. J. 91, 600-607
44. Petrache, H. I., Tristram-Nagle, S., Gawrisch, K., Harries, D., Parsegian, V. A., and Nagle, J. F. (2004) Structure and fluctuations of charged phosphatidylserine bilayers in the absence of salt. Biophys. J. 86, 1574-1586 (Pubitemid 38304847)
45. Xie, X. Q., Chen, J. Z., and Billings, E. M. (2003) Three-dimensional structural model of the G-protein-coupled cannabinoid CB2 receptor. Proteins 53, 307-319
46. Thomas, B. F., Compton, D. R., and Martin, B. R. (1990) Characterization of the lipophilicity of natural and synthetic analogs of δ9- tetrahydrocannabinol and its relationship to pharmacological potency. J. Pharmacol. Exp. Ther. 255, 624-630
47. Shoemaker, J. L., Ruckle, M. B., Mayeux, P. R., and Prather, P. L. (2005) Agonist-directed trafficking of response by endocannabinoids acting at CB2 receptors. J. Pharmacol. Exp. Ther. 315, 828-838 (Pubitemid 41509039)
48. Hafez, I. M., and Cullis, P. R. (2000) Cholesteryl hemisuccinate exhibits pH-sensitive polymorphic phase behavior. Biochim. Biophys. Acta 1463, 107-114 (Pubitemid 30019240)
49. Farrens, D. L., Altenbach, C., Yang, K., Hubbell, W. L., and Khorana, H. G. (1996) Requirement of rigid-body motion of transmembrane helices for light activation of rhodopsin. Science 274, 768-770 (Pubitemid 26398253)
50. Mitchell, D. C., Straume, M., Miller, J. L., and Litman, B. J. (1990) Modulation of metarhodopsin formation by cholesterol-induced ordering of bilayer lipids. Biochemistry 29, 9143-9149 (Pubitemid 20320878)
51. 2 receptor signaling and 2-arachidonoyl-glycerol metabolism in human immune cells. J. Immunol. 177, 4971-4980
52. Bari, M., Battista, N., Fezza, F., Finazzi-Agrò, A., and Maccarrone, M. (2005) Lipid rafts control signaling of type-1 cannabinoid receptors in neuronal cells. Implications for anandamide-induced apoptosis. J. Biol. Chem. 280, 12212-12220
53. Bari, M., Paradisi, A., Pasquariello, N., and Maccarrone, M. (2005) Cholesterol- dependent modulation of type 1 cannabinoid receptors in nerve cells. J. Neurosci. Res. 81, 275-283 (Pubitemid 41153342)
54. Sarnataro, D., Grimaldi, C., Pisanti, S., Gazzerro, P., Laezza, C., Zurzolo, C., and Bifulco, M. (2005) Plasma membrane and lysosomal localization of CB1 cannabinoid receptor are dependent on lipid rafts and regulated by anandamide in human breast cancer cells. FEBS Lett. 579, 6343-6349 (Pubitemid 41612150)
55. Bari, M., Oddi, S., De Simone, C., Spagnolo, P., Gasperi, V., Battista, N., Centonze, D., and Maccarrone, M. (2008) Type-1 cannabinoid receptors colocalize with caveolin-1 in neuronal cells. Neuropharmacology 54, 45-50 (Pubitemid 350299413)
56. Cevc, G., Watts, A., and Marsh, D. (1981) Titration of the phase transition of phosphatidylserine bilayer membranes. Effects of pH, surface electrostatics, ion binding, and head group hydration. Biochemistry 20, 4955-4965
57. Roy, M. T., Gallardo, M., and Estelrich, J. (1998) Influence of size on electrokinetic behavior of phosphatidylserine and phosphatidylethanolamine lipid vesicles. J. Colloid Interface Sci. 206, 512-517 (Pubitemid 28469190)
58. Chen, N. R., and Ho, J. T. (1985) Raman study of effect of phospholipid chain unsaturation on bilayer phase transitions. Biochem. Biophys. Res. Commun. 127, 220-225
59. 13C NMR study on the binding state in large unilamellar vesicles. Biochemistry 45, 15601-15609
60. Krishna, A. G., Menon, S. T., Terry, T. J., and Sakmar, T. P. (2002) Evidence that helix 8 of rhodopsin acts as a membrane-dependent conformational switch. Biochemistry 41, 8298-8309 (Pubitemid 34705483)
61. Mozsolits, H., Unabia, S., Ahmad, A., Morton, C. J., Thomas, W. G., and Aguilar, M. I. (2002) Electrostatic and hydrophobic forces tether the proximal region of the angiotensin II receptor (AT1A) carboxyl terminus to anionic lipids. Biochemistry 41, 7830-7840 (Pubitemid 34627810)
62. Scheerer, P., Park, J. H., Hildebrand, P. W., Kim, Y. J., Krauss, N., Choe, H. W., Hofmann, K. P., and Ernst, O. P. (2008) Crystal structure of opsin in its G-protein-interacting conformation. Nature 455, 497-502
63. Choe, H. W., Kim, Y. J., Park, J. H., Morizumi, T., Pai, E. F., Krauss, N., Hofmann, K. P., Scheerer, P., and Ernst, O. P. (2011) Crystal structure of metarhodopsin II. Nature 471, 651-655
64. Grace, C. R., Cowsik, S. M., Shim, J. Y., Welsh, W. J., and Howlett, A. C. (2007) Unique helical conformation of the fourth cytoplasmic loop of the CB1 cannabinoid receptor in a negatively charged environment. J. Struct. Biol. 159, 359-368 (Pubitemid 47354228)
65. 1 cannabinoid receptor using NMR and circular dichroism. Biochim. Biophys. Acta 1668, 1-9
66. 2receptors in membrane mimetic dodecylphosphocholine micelles. J. Biol. Chem. 280, 3605-3612
67. Hurst, D. P., Grossfield, A., Lynch, D. L., Feller, S., Romo, T. D., Gawrisch, K., Pitman, M. C., and Reggio, P. H. (2010) A lipid pathway for ligand binding is necessary for a cannabinoid G protein-coupled receptor. J. Biol. Chem. 285, 17954-17964
68. Escribá, P. V., Ozaita, A., Ribas, C., Miralles, A., Fodor, E., Farkas, T., and García-Sevilla, J. A. (1997) Role of lipid polymorphism in G protein-membrane interactions. Nonlamellar-prone phospholipids and peripheral protein binding to membranes. Proc. Natl. Acad. Sci. U.S.A. 94, 11375-11380
69. Kosloff, M., Alexov, E., Arshavsky, V. Y., and Honig, B. (2008) Electrostatic and lipid anchor contributions to the interaction of transducin with membranes. Mechanistic implications for activation and translocation. J. Biol. Chem. 283, 31197-31207
70. van Meer, G., Voelker, D. R., and Feigenson, G. W. (2008) Membrane lipids. Where they are and how they behave. Nat. Rev. Mol. Cell. Biol. 9, 112-124 (Pubitemid 351158912)
71. Zachowski, A. (1993) Phospholipids in animal eukaryotic membranes. Transverse asymmetry and movement. Biochem. J. 294, 1-14
72. Galiègue, S., Mary, S., Marchand, J., Dussossoy, D., Carrière, D., Carayon, P., Bouaboula, M., Shire, D., Le Fur, G., and Casellas, P. (1995) Expression of central and peripheral cannabinoid receptors in human immune tissues and leukocyte subpopulations. Eur. J. Biochem. 232, 54-61
73. Callahan, M. K., Williamson, P., and Schlegel, R. A. (2000) Surface expression of phosphatidylserine on macrophages is required for phagocytosis of apoptotic thymocytes. Cell Death Differ. 7, 645-653 (Pubitemid 30456170)
74. Dillon, S. R., Mancini, M., Rosen, A., and Schlissel, M. S. (2000) Annexin V binds to viable B cells and colocalizes with a marker of lipid rafts upon B cell receptor activation. J. Immunol. 164, 1322-1332 (Pubitemid 30067245)
75. Appelt, U., Sheriff, A., Gaipl, U. S., Kalden, J. R., Voll, R. E., and Herrmann, M. (2005) Viable, apoptotic, and necrotic monocytes expose phosphatidylserine. Cooperative binding of the ligand annexin V to dying but not viable cells and implications for PS-dependent clearance. Cell Death Differ. 12, 194-196 (Pubitemid 40220651)
76. Berger, C., Ho, J. T., Kimura, T., Hess, S., Gawrisch, K., and Yeliseev, A. (2010) Protein Exp. Purif. 70, 236-247
77. 2 cannabinoid receptor. Biochemistry 47, 13811-13821
78. 2H nuclear magnetic resonance order parameter profiles suggest a change of molecular shape for phosphatidylcholines containing a polyunsaturated acyl chain. Biophys. J. 68, 2396-2403
79. Polozov, I. V., and Gawrisch, K. (2006) Characterization of the liquid-ordered state by proton MAS NMR. Biophys. J. 90, 2051-2061